The Role of PHT1 Family Transporters in the Acquisition and Redistribution of Phosphorus in Plants

[en] Phosphorus (P) is one of the most important macronutrients for plant growth and yield. Low availability of inorganic phosphate (Pi) in soil substantially curbs crop production, whereas excessive Pi fertilization causes economic and ecological problems. The rapid depletion of global rock phosphate (RP) reserves calls for efficient plant Pi-management. To cope with low Pi (LP) stress, plants have evolved morphological, physiological, molecular, and biochemical adaptations. Apart from arbuscular mycorrhizal fungi (AMF)-mediated Pi acquisition, Pi uptake, it's export, utilization, and remobilization depend on transport processes mediated by membrane bound PHosphate Transporters (PHTs), which are grouped into five families. Among these, the PHT1 family is the primary transporter involved in the acquisition of Pi from soil and redistribution within plants. In this review, we present a brief account on 5 PHTs (PHT1 to PHT5) and focus on PHT1s. We cover in detail the PHT1s identified and characterized until now in various plants including their phylogenetic relationships, induction by AMF, localization, and affinity. We also discuss the extant understanding of the regulation of PHT1s at transcriptional, post-transcriptional, and post-translational levels. Further exploitation of PHT1s will help overcome the problems associated with LP soils and assist in improving crop yields through sustainable agriculture. © 2019, © 2019 Taylor & Francis Group, LLC.

Disciplines :

Biotechnology

Author, co-author :

Victor Roch, G.; Division of Plant Biotechnology, Entomology Research Institute, Loyola College, Chennai, India

Maharajan, T.; Division of Plant Biotechnology, Entomology Research Institute, Loyola College, Chennai, India

Stanislaus, Antony Ceasar ; Université de Liège - ULg

Ignacimuthu, S.; Division of Plant Biotechnology, Entomology Research Institute, Loyola College, Chennai, India, St. Xavier’s College, Palyamkottai, India

Language :

English

Title :

The Role of PHT1 Family Transporters in the Acquisition and Redistribution of Phosphorus in Plants

Publication date :

2019

Journal title :

Critical Reviews in Plant Sciences

ISSN :

0735-2689

eISSN :

1549-7836

Publisher :

Taylor & Francis, United Kingdom

Volume :

Issue :

Pages :

171-198

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 20 July 2021

Statistics

Number of views

85 (1 by ULiège)

Number of downloads

1 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

102

Bibliography

Ai, P., Sun, S., Zhao, J., Fan, X., Xin, W., Guo, Q., Yu, L., Shen, Q., Wu, P., and Miller, A. J., 2009. Two rice phosphate transporters, OsPht1; 2 and OsPht1; 6, have different functions and kinetic properties in uptake and translocation. Plant J. 57: 798–809.
Alatorre-Cobos, F., López-Arredondo, D., and Herrera-Estrella, L., 2009. Genetic determinants of phosphate use efficiency in crops. In Genes for Plant Abiotic Stress; Jenks, M. A., and Wood, A. J., Eds. Wiley-Blackwell: Oxford, pp 143–165.
Arpat, A. B., Magliano, P., Wege, S., Rouached, H., Stefanovic, A., and Poirier, Y., 2012. Functional expression of PHO1 to the Golgi and trans‐Golgi network and its role in export of inorganic phosphate. Plant J. 71: 479–491.
Ayadi, A., David, P., Arrighi, J. F., Chiarenza, S., Thibaud, M. C., Nussaume, L., and Marin, E., 2015. Reducing the genetic redundancy of Arabidopsis PHT1 transporters to study phosphate uptake and signaling. Plant Physiol. 167: 1511–1526.
Aziz, T., Finnegan, P. M., Lambers, H., and Jost, R., 2014. Organ‐specific phosphorus‐allocation patterns and transcript profiles linked to phosphorus efficiency in two contrasting wheat genotypes. Plant Cell Environ. 37: 943–960.
Baker, A., Ceasar, S. A., Palmer, A. J., Paterson, J. B., Qi, W., Muench, S. P., and Baldwin, S. A., 2015. Replace, reuse, recycle: improving the sustainable use of phosphorus by plants. J. Exp. Bot. 66: 3523–3540.
Bao, S., An, L., Su, S., Zhou, Z., and Gan, Y., 2011. Expression patterns of nitrate, phosphate, and sulfate transporters in Arabidopsis roots exposed to different nutritional regimes. Botany 89: 647–653.
Bayle, V., Arrighi, J. F., Creff, A., Nespoulous, C., Vialaret, J., Rossignol, M., Gonzalez, E., Paz-Ares, J., and Nussaume, L., 2011. Arabidopsis thaliana high-affinity phosphate transporters exhibit multiple levels of posttranslational regulation. Plant Cell. 23: 1523–1535.
Berndt, T., and Kumar R., 2009. Novel mechanisms in the regulation of phosphorus homeostasis. Physiol. 24: 17–25.
Bieleski, R. 1973. Phosphate pools, phosphate transport, and phosphate availability. Ann. Rev. Plant Physiol. 24: 225–252.
Boico, I. 2015. Arabidopsis thaliana High Affinity Phosphate Transporters PHT1; 8 and PHT1; 9 are Important for Adaptation to Pi Stress. PhD thesis, North Carolina State University, Raleigh, North Carolina.
Bustos, R., Castrillo, G., Linhares, F., Puga, M. I., Rubio, V., Pérez-Pérez, J., Solano, R., Leyva, A., and Paz-Ares, J., 2010. A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet. 6: e1001102.
Carroll, S. B., 2005. Evolution at two levels: on genes and form. PLoS Biol. 3: e245.
Castrillo, G, Turck, F., Leveugle, M., Lecharny, A., Carbonero, P., Coupland, G., Paz-Ares, J., and Oñate-Sánchez, L., 2011. Functional characterization of the PHT1 family transporters of foxtail millet with development of a novel Agrobacterium-mediated transformation procedure. PLoS One 6: e21524.
Castrillo, G., Sánchez-Bermejo, E., de Lorenzo, L., Crevillén, P., Fraile-Escanciano, A., Mohan, T., Mouriz, A., Catarecha, P., Sobrino-Plata, J., and Olsson, S., 2013. WRKY6 transcription factor restricts arsenate uptake and transposon activation in Arabidopsis. Plant Cell 25: 2944–2957.
Catarecha, P., Segura, M. D., Franco-Zorrilla, J. M., García-Ponce, B., Lanza, M., Solano, R., Paz-Ares, J., and Leyva, A., 2007. A mutant of the Arabidopsis phosphate transporter PHT1; 1 displays enhanced arsenic accumulation. Plant Cell 19: 1123–1133.
Ceasar, S. A., Hodge, A., Baker, A., and Baldwin, S. A., 2014. Phosphate concentration and arbuscular mycorrhizal colonisation influence the growth, yield and expression of twelve PHT1 family phosphate transporters in foxtail millet (Setaria italica). PLoS One 9: e108459.
Ceasar, S. A., Baker, A., Muench, S. P., Ignacimuthu, S., and Baldwin, S. A., 2016. The conservation of phosphate-binding residues among PHT1 transporters suggests that distinct transport affinities are unlikely to result from differences in the phosphate-binding site. Biochem. Soc. Trans. 44: 1541–1548.
Ceasar, S. A., Baker, A., and Ignacimuthu, S., 2017. Functional characterization of the PHT1 family transporters of foxtail millet with development of a novel Agrobacterium-mediated transformation procedure. Sci. Rep. 7: 14064.
Ceasar S. A., Maharajan, T., Krishna, T. A., Ramakrishnan, M., Roch, G. V., Satish, L., and Ignacimuthu, S., 2018. Finger millet [Eleusine coracana (L.) Gaertn.] improvement: current status and future interventions of whole genome sequence. Front. Plant Sci. 9: 1054.
Ceasar S. A., 2018a. Feeding world population amidst depleting phosphate reserves: the role of biotechnological interventions. Open Biotechnol. J. 12: 51–55.
Ceasar S. A., 2018b. Genome-wide identification and in silico analysis of PHT1 family genes and proteins in Setaria viridis: the best model to study nutrient transport in millets. Plant Genome. 12: 1–9.
Chang, M., Gu, M., Xia, Y., Dai, X., Dai, C., Zhang, J., Wang, S., Qu, H., Yamaji, N., and Ma, J. F., 2019. OsPHT1; 3 mediates uptake, translocation and remobilization of phosphate under extremely low phosphate regimes. Plant Physiol. 179: 656–670.
Chen, Z. H., Nimmo, G. A., Jenkins, G. I., and Nimmo, H. G., 2007. BHLH32 modulates several biochemical and morphological processes that respond to Pi starvation in Arabidopsis. Biochem. J. 405: 14064–14198.
Chen, A., Hu, J., Sun, S., and Xu, G., 2007 Conservation and divergence of both phosphate‐and mycorrhiza‐regulated physiological responses and expression patterns of phosphate transporters in solanaceous species. New Phytol. 173: 817–831.
Chen, Y. F., Li, L. Q., Xu, Q., Kong, Y. H., Wang, H., and Wu, W. H., 2009. The WRKY6 transcription factor modulates Phosphate1 expression in response to low Pi stress in Arabidopsis. Plant Cell. 21: 3554–3566.
Chen, A., Gu, M., Sun, S., Zhu, L., Hong, S., and Xu. G., 2011a. Identification of two conserved cis‐acting elements, MYCS and P1BS, involved in the regulation of mycorrhiza‐activated phosphate transporters in eudicot species. New Phytol. 189: 1157–1169.
Chen, J., Liu, Y., Ni, J., Wang, Y., Bai, Y., Shi, J., Gan, J., Wu, Z., and Wu, P., 2011b. OsPHF1 regulates the plasma membrane localization of low-and high-affinity inorganic phosphate transporters and determines inorganic phosphate uptake and translocation in rice. Plant Physiol. 157: 269–278.
Chen, A., Chen, X., Wang, H., Liao, D., Gu, M., Qu, H., Sun, S., and Xu, G., 2014. Genome-wide investigation and expression analysis suggest diverse roles and genetic redundancy of Pht1 family genes in response to Pi deficiency in tomato. BMC Plant Biol. 14: 61.
Chen, C. Y., and Schmidt, W., 2015. The paralogous R3 MYB proteins CAPRICE, TRIPTYCHON and enhancer of try and CPC1 play pleiotropic and partly non-redundant roles in the phosphate starvation response of Arabidopsis roots. J. Exp. Bot. 66: 4821–4834.
Chen, J., Wang, Y., Wang, F., Yang, J., Gao, M., Li, C., Liu, Y., Liu, Y., Yamaji, N., and Ma, J. F., 2015. The rice CK2 kinase regulates trafficking of phosphate transporters in response to phosphate levels. Plant Cell. 27: 711–723.
Chiou, T. J., Liu, H., and Harrison, M. J., 2001. The spatial expression patterns of a phosphate transporter (MtPT1) from Medicago truncatula indicate a role in phosphate transport at the root/soil interface. Plant J. 25: 281–293.
Chiou, T. J., Aung, K., Lin, S. I., Wu, C. C., Chiang, S. F., and Su, C. l., 2006. Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell. 18: 412–421.
Consortium, IBGS., 2012. A physical, genetic and functional sequence assembly of the barley genome. Nature 491: 711–716.
Cubero, B., Nakagawa, Y., Jiang, X. Y., Miura, K. J., Li, F., Raghothama, K. G., Bressan, R. A., Hasegawa, P. M., and Pardo J. M., 2009. The phosphate transporter PHT4; 6 is a determinant of salt tolerance that is localized to the Golgi apparatus of Arabidopsis. Mol. Plant. 2: 535–552.
Dai, X., Wang, Y., Yang, A., and Zhang, W. H., 2012. OsMYB2P-1, a R2R3 MYB transcription factor, is involved in regulation of phosphate-starvation responses and root architecture in rice. Plant Physiol. 159: 169–183.
Deng, Y., Chen, K., Teng, W., Zhan, A., Tong, Y., Feng, G., Cui, Z., Zhang, F., and Chen, X., 2014. Is the inherent potential of maize roots efficient for soil phosphorus acquisition? PLoS One 9: e90287.
Devaiah, B. N., Karthikeyan, A. S., and Raghothama, K. G., 2007a. WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol. 143: 1789–1801.
Devaiah, B. N., Nagarajan, V. K., and Raghothama, K. G., 2007b. Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6. Plant Physiol. 145: 147–159.
Devaiah, B. N., Madhuvanthi, R., Karthikeyan, A. S., and Raghothama K. G., 2009. Phosphate starvation responses and gibberellic acid biosynthesis are regulated by the MYB62 transcription factor in Arabidopsis. Mol. Plant. 2: 43–58.
Ding, W., Wang, Y., Fang, W., Gao, S., Li, X., and Xiao, K., 2016. TaZAT8, a C2H2‐ZFP type transcription factor gene in wheat, plays critical roles in mediating tolerance to Pi deprivation through regulating P acquisition, ROS homeostasis and root system establishment. Physiol. Plant. 158: 297–311.
DiTusa, S. F., Fontenot, E. B., Wallace, R. W., Silvers, M. A., Steele, T. N., Elnagar, A. H., Dearman, K. M., and Smith, A. P., 2016. A member of the Phosphate transporter 1 (Pht1) family from the arsenic‐hyperaccumulating fern Pteris vittata is a high‐affinity arsenate transporter. New Phytolo. 209: 762–772.
Driessen, P., Deckers, J., Spaargaren, O., and Nachtergaele, F., 2000. Lecture notes on the major soils of the world. Food and Agriculture Organization (FAO), Rome. 94, pp 35–37.
Druka, A., Muehlbauer, G., Druka, I., Caldo, R., Baumann, U., Rostoks, N., Schreiber, A., Wise, R., Close, T., and Kleinhofs, A., 2006. An atlas of gene expression from seed to seed through barley development. Funct. Integr. Genomics. 6: 202–211.
Duan, K., Yi, K., Dang, L., Huang, H., Wu, W., and Wu, P., 2008. Characterization of a sub‐family of Arabidopsis genes with the SPX domain reveals their diverse functions in plant tolerance to phosphorus starvation. Plant J. 54: 965–975.
Fan, C., Wang, X., Hu, R., Wang, Y., Xiao, C., Jiang, Y., Zhang, X., Zheng, C., and Fu, Y. F., 2013. The pattern of Phosphate transporter 1 genes evolutionary divergence in Glycine max L. BMC Plant Biol. 13: 48.
Forrest, L. R., Krämer, R., and Ziegler, C., 2011. The structural basis of secondary active transport mechanisms. Biochim. Biophys. Acta Bioenerg. 1807: 167–188.
Fujii, H., Chiou, T. J., Lin, S. I., Aung, K., and Zhu, J. K., 2005. A miRNA involved in phosphate-starvation response in Arabidopsis. Curr. Biol. 15: 2038–2043.
Gahoonia, T. S., and Nielsen, N. E., 1997. Variation in root hairs of barley cultivars doubled soil phosphorus uptake. Euphytica. 98: 177–182.
Gamuyao, R., Chin, J. H., Pariasca-Tanaka, J., Pesaresi, P., Catausan, S., Dalid, C., Slamet-Loedin, I., Tecson-Mendoza, E. M., Wissuwa, M., and Heuer, S., 2012. The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature 488: 535–541.
Gaxiola, R. A., Edwards, M., and Elser, J. J., 2011. A transgenic approach to enhance phosphorus use efficiency in crops as part of a comprehensive strategy for sustainable agriculture. Chemosphere. 84: 840–845.
Glassop, D., Smith, S. E., and Smith, F. W., 2005. Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222: 688–698.
Glassop, D., Godwin, R. M., Smith, S. E., and Smith, F. W., 2007. Rice phosphate transporters associated with phosphate uptake in rice roots colonised with arbuscular mycorrhizal fungi. Botany 85: 644–651.
Gomez-Ariza, J., Balestrini, R., Novero, M., and Bonfante, P., 2009. Cell-specific gene expression of phosphate transporters in mycorrhizal tomato roots. Biol. Fert. Soils. 45: 845–853.
González, E., Solano, R., Rubio, V., Leyva, A., and Paz-Ares, J., 2005. Phosphate transporter traffic facilitator 1 is a plant-specific SEC12-related protein that enables the endoplasmic reticulum exit of a high-affinity phosphate transporter in Arabidopsis. Plant Cell. 17: 3500–3512.
Grün, A., Buchner, P., Broadley, M., and Hawkesford, M., 2018. Identification and expression profiling of Pht1 phosphate transporters in wheat in controlled environments and in the field. Plant Biol. 20: 374–389.
Grunwald, U., Guo, W., Fischer, K., Isayenkov, S., Ludwig-Müller, J., Hause, B., Yan, X., Küster, H., and Franken, P., 2009. Overlapping expression patterns and differential transcript levels of phosphate transporter genes in arbuscular mycorrhizal, Pi-fertilised and phytohormone-treated Medicago truncatula roots. Planta 229: 1023–1034.
Gu, M., Liu, W., Meng, Q., Zhang, W., Chen, A., Sun, S., and Xu, G., 2014. Identification of microRNAs in six solanaceous plants and their potential link with phosphate and mycorrhizal signaling. J. Integr. Plant Biol. 56: 1164–1178.
Gu, M., Chen, A., Sun, S., and Xu, G., 2016. Complex regulation of plant phosphate transporters and the gap between molecular mechanisms and practical application: what is missing? Mol. Plant 9: 396–416.
Güimil, S., Chang, H. S., Zhu, T., Sesma, A., Osbourn, A., Roux, C., Ioannidis, V., Oakeley, E. J., Docquier, M., and Descombes P., 2005. Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc. Natl. Acad. Sci. 102: 8066–8070.
Guo, B., Irigoyen, S., Fowler, T. B., and Versaw, W. K., 2008a. Differential expression and phylogenetic analysis suggest specialization of plastid-localized members of the PHT4 phosphate transporter family for photosynthetic and heterotrophic tissues. Plant Signaling. Behav. 3: 784–790.
Guo, B., Jin, Y., Wussler, C., Blancaflor, E., Motes, C., and Versaw, W. K., 2008b. Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters. New Phytol. 177: 889–898.
Guo, C., Zhao, X., Liu, X., Zhang, L., Gu, J., Li, X., Lu, W., and Xiao, K., 2013. Function of wheat phosphate transporter gene TaPHT2; 1 in Pi translocation and plant growth regulation under replete and limited Pi supply conditions. Planta 237: 1163–1178.
Guo, C., Guo, L., Li, X., Gu, J., Zhao, M., Duan, W., Ma, C., Lu, W., and Xiao, K., 2014. TaPT2, a high-affinity phosphate transporter gene in wheat (Triticum aestivum L.), is crucial in plant Pi uptake under phosphorus deprivation. Acta Physiol. Plant. 36: 1373–1384.
Hackenberg, M., Shi, B. J., Gustafson, P., and Langridge, P., 2013. Characterization of phosphorus-regulated miR399 and miR827 and their isomirs in barley under phosphorus-sufficient and phosphorus-deficient conditions. BMC Plant Biol. 13: 214.
Hamburger, D., Rezzonico, E., Petétot, J. M. C., Somerville, C., and Poirier, Y., 2002. Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell. 14: 889–902.
Hamel, P., Saint‐Georges, Y., De Pinto, B., Lachacinski, N., Altamura, N., and Dujardin, G., 2004. Redundancy in the function of mitochondrial phosphate transport in Saccharomyces cerevisiae and Arabidopsis thaliana. Mol. Microbiol. 51: 307–317.
Hammond, J. P., and White, P. J., 2008. Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J. Exp. Bot. 59: 93–109.
Harrison, M. J., Dewbre, G. R., and Liu, J., 2002. A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell. 14: 2413–2429.
Hatakeyama, M., Aluri, S., Balachadran, M. T., Sivarajan, S. R., Patrignani, A., Grüter, S., Poveda, L., Shimizu-Inatsugi, R., Baeten, J., and Francoijs, K. J., 2017. Multiple hybrid de novo genome assembly of finger millet, an orphan allotetraploid crop. DNA Res. 25: 39–47.
Hildebrandt, U., Janetta, K., and Bothe, H., 2002. Towards growth of arbuscular mycorrhizal fungi independent of a plant host. Appl. Environ. Microbiol. 68: 1919–1924.
Himelblau, E., and Amasino, R. M., 2001. Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence. J. Plant Physiol. 158: 1317–1323.
Hirsch, J., Marin, E., Floriani, M., Chiarenza, S., Richaud, P., Nussaume, L., and Thibaud M., 2006. Phosphate deficiency promotes modification of iron distribution in Arabidopsis plants. Biochimie. 88: 1767–1771.
Hittalmani, S., Mahesh, H., Shirke, M. D., Biradar, H., Uday, G., Aruna, Y., Lohithaswa, H., and Mohanrao, A., 2017. Genome and transcriptome sequence of finger millet (Eleusine coracana (L.) Gaertn.) provides insights into drought tolerance and nutraceutical properties. BMC Genomics. 18: 465.
Hong, J. J., Park, Y. S., Bravo, A., Bhattarai, K. K., Daniels, D. A., and Harrison, M. J., 2012. Diversity of morphology and function in arbuscular mycorrhizal symbioses in Brachypodium distachyon. Planta 236: 851–865.
Horst, W. J., Abdou, M., and Wiesler, F., 1996. Differences between wheat cultivars in acquisition and utilization of phosphorus. J. Plant Nutr. Soil Sci. 159: 155–161.
Huang, C. Y., Roessner, U., Eickmeier, I., Genc, Y., Callahan, D. L., Shirley, N., Langridge, P., and Bacic, A., 2008. Metabolite profiling reveals distinct changes in carbon and nitrogen metabolism in phosphate-deficient barley plants (Hordeum vulgare L.). Plant Cell Physiol. 49: 691–703.
Huang, C. Y., Shirley, N., Genc, Y., Shi, B., and Langridge, P., 2011. Phosphate utilization efficiency correlates with expression of low-affinity phosphate transporters and non-coding RNA, IPS1 in barley. Plant Physiol. 156: 1217–1229.
Huang, T. K., Han, C. L., Lin, S. I., Chen, Y. J., Tsai, Y. C., Chen, Y. R., Chen, J. W., Lin, W. Y., Chen, P. M., and Liu T. Y., 2013. Identification of downstream components of ubiquitin-conjugating enzyme phosphate 2 by quantitative membrane proteomics in Arabidopsis roots. Plant Cell. 25: 4044–4060.
Initiative, A, G., 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.
Inoue, Y., Kobae, Y., Omoto, E., Tanaka, A., Banba, M., Takai, S., Tamura, Y., Hirose, A., Komatsu, K., and Otagaki, S., 2014. The soybean mycorrhiza-inducible phosphate transporter gene, GmPT7, also shows localized expression at the tips of vein endings of senescent leaves. Plant. Cell Physiol. 55: 2102–2111.
Jain, A., Nagarajan, V. K., and Raghothama, K. G., 2012. Transcriptional regulation of phosphate acquisition by higher plants. Cell. Mol. Life Sci. 69: 3207–3224.
Javot, H., Penmetsa, R. V., Terzaghi, N., Cook, D. R., and Harrison, M. J., 2007. A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. 104: 1720–1725.
Jewell, M. C., Campbell, B. C., and Godwin, I. D., 2010. Transgenic plants for abiotic stress resistance. In Transgenic Crop Plants; Chittaranjan, K., Charles, H. M., Albert, G. A., and Timothy, C. H., Eds. Springer-Verlag Berlin Heidelberg: Heidelberg, Germany, pp 67–132.
Jia, H., Ren, H., Gu, M., Zhao, J., Sun, S., Zhang, X., Chen, J., Wu, P., and Xu, G., 2011. The phosphate transporter gene OsPht1; 8 is involved in phosphate homeostasis in rice. Plant Physiol. 156: 1164–1175.
Jia, F., Wan, X., Zhu, W., Sun, D., Zheng, C., Liu, P., and Huang, J., 2015. Overexpression of mitochondrial phosphate transporter 3 severely hampers plant development through regulating mitochondrial function in Arabidopsis. PLoS One 10: e0129717.
Jones, D. T., Taylor, W. R., and Thornton, J. M. 1992. The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8: 275–282.
Julia, C. C., Rose, T. J., Pariasca-Tanaka, J., Jeong, K., Masuda, T., and Wissuwa, M., 2018. Phosphorus uptake commences at the earliest stages of seedling development in rice (Oryza sativa L.). J. Exp. Bot. 69: 5233–5240.
Karthikeyan, A. S., Varadarajan, D. K., Mukatira, U. T., D'Urzo, M. P., Damsz, B., and Raghothama, K. G., 2002. Regulated expression of Arabidopsis phosphate transporters. Plant Physiol. 130: 221–233.
Karthikeyan, A. S., Varadarajan, D. K., Jain, A., Held, M. A., Carpita, N. C., and Raghothama, K. G., 2007. Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta 225: 907–918.
Koide, R., and Kabir, Z., 2000. Extraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. New Phytol. 148: 511–517.
Kuo, H. F., and Chiou, T. J., 2011. The role of microRNAs in phosphorus deficiency signaling. Plant Physiol. 156: 1016–1024.
Lapis-Gaza, H. R., Jost, R., and Finnegan, P. M., 2014. Arabidopsis phosphate transporter1 genes PHT1; 8 and PHT1; 9 are involved in root-to-shoot translocation of orthophosphate. BMC Plant Biol. 14: 334.
Leggewie, G., Willmitzer, L., and Riesmeier, J. W., 1997. Two cDNAs from potato are able to complement a phosphate uptake-deficient yeast mutant: identification of phosphate transporters from higher plants. Plant Cell. 9: 381–392.
Li, Z., Gao, Q., Liu, Y., He, C., Zhang, X., and Zhang, J., 2011. Overexpression of transcription factor ZmPTF1 improves low phosphate tolerance of maize by regulating carbon metabolism and root growth. Planta 233: 1129–1143.
Li, Y., Zhang, J., Zhang, X., Fan, H., Gu, M., Qu, H., and Xu, G., 2015. Phosphate transporter OsPht1; 8 in rice plays an important role in phosphorus redistribution from source to sink organs and allocation between embryo and endosperm of seeds. Plant Sci. 230: 23–32.
Lin, W. Y., Huang, T. K., and Chiou, T. J., 2013. Nitrogen limitation adaptation, a target of microRNA827, mediates degradation of plasma membrane–localized phosphate transporters to maintain phosphate homeostasis in Arabidopsis. Plant Cell. 25: 4061–4074.
Liu, C., Muchhal, U. S., Uthappa, M., Kononowicz, A. K., and Raghothama, K. G., 1998a. Tomato phosphate transporter genes are differentially regulated in plant tissues by phosphorus. Plant Physiol. 116: 91–99.
Liu, H., Trieu, A. T., Blaylock, L. A., and Harrison, M. J., 1998b. Cloning and characterization of two phosphate transporters from Medicago truncatula roots: regulation in response to phosphate and to colonization by arbuscular mycorrhizal (AM) fungi. Mol. Plant-Microbe Interact. 11: 14–22.
Liu, J., Samac, D. A., Bucciarelli, B., Allan, D. L., and Vance, C. P., 2005. Signaling of phosphorus deficiency‐induced gene expression in white lupin requires sugar and phloem transport. Plant J. 41: 257–268.
Liu, J., Versaw, W. K., Pumplin, N., Gomez, S. K., Blaylock, L. A., and Harrison, M. J., 2008. Closely related members of the Medicago truncatula PHT1 phosphate transporter gene family encode phosphate transporters with distinct biochemical activities. J. Biol. Chem. 283: 24673–24681.
Liu, F., Chang, X. J., Ye, Y., Xie, W. B., Wu, P., and Lian, X. M., 2011a. Comprehensive sequence and whole-life-cycle expression profile analysis of the phosphate transporter gene family in rice. Mol. Plant. 4: 1105–1122.
Liu, T. Y., Aung, K., Tseng, C. Y., Chang, T. Y., Chen, Y. S., and Chiou, T. J., 2011b. Vacuolar Ca2+/H+ transport activity is required for systemic phosphate homeostasis involving shoot-to-root signaling in Arabidopsis. Plant Physiol. 156: 1176–1189.
Liu, T. Y., Huang, T. K., Tseng, C. Y., Lai, Y. S., Lin, S. I., Lin, W. Y., Chen, J. W., and Chiou, T. J., 2012. PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis. Plant Cell. 24: 2168–2183.
Liu, X., Zhao, X., Zhang, L., Lu, W., Li, X., and Xiao, K., 2013. TaPht1; 4, a high-affinity phosphate transporter gene in wheat (Triticum aestivum), plays an important role in plant phosphate acquisition under phosphorus deprivation. Funct. Plant Biol. 40: 329–341.
Liu, P., Chen, S., Song, A., Zhao, S., Fang, W., Guan, Z., Liao, Y., Jiang, J., and Chen, F., 2014. A putative high affinity phosphate transporter, CmPT1, enhances tolerance to Pi deficiency of chrysanthemum. BMC Plant Biol. 14: 18.
Liu, F., Xu, Y., Jiang, H., Jiang, C., Du, Y., Gong, C., Wang, W., Zhu, S., Han, G., and Cheng, B., 2016a. Systematic identification, evolution and expression analysis of the Zea mays PHT1 gene family reveals several new members involved in root colonization by arbuscular mycorrhizal fungi. Int. J. Mol. Sci. 17: 930.
Liu, T. Y., Huang, T. K., Yang, S. Y., Hong, Y. T., Huang, S. M., Wang, F. N., Chiang, S. F., Tsai, S. Y., Lu, W. C., and Chiou, T. J., 2016b. Identification of plant vacuolar transporters mediating phosphate storage. Nat. Commun. 7: 11095.
Liu, B., Zhao, S., Wu, X., Wang, X., Nan, Y., Wang, D., and Chen, Q., 2017. Identification and characterization of phosphate transporter genes in potato. J. Biotechnol. 264: 17–28.
López-Arredondo, D. L., Leyva-González, M. A., González-Morales, S. I., and López-Bucio, J., Herrera-Estrella, L., 2014. Phosphate nutrition: improving low-phosphate tolerance in crops. Annu. Rev. Plant Biol. 65: 95–123.
Lota, F., Wegmüller, S., Buer, B., Sato, S., Bräutigam, A., Hanf, B., and Bucher, M., 2013. The cis‐acting CTTC–P1 BS module is indicative for gene function of L j VTI 12, a Q b‐SNARE protein gene that is required for arbuscule formation in Lotus japonicus. Plant J. 74: 280–293.
Lu, Q., Zhao, J., Tian, J., Chen, L., Sun, Z., Guo, Y., Lu, X., Gu, M., Xu, G., and Liao H., 2012. The high-affinity phosphate transporter GmPT5 regulates phosphate transport to nodules and nodulation in soybean. Plant Physiol. 159: 1634–1643.
Luan, M., Zhao, F., Han, X., Sun, G., Yang, Y., Liu, J., Shi, J., Fu, A., Lan, W., and Luan, S., 2019. Vacuolar phosphate transporters contribute to systemic phosphate homeostasis vital for reproductive development in Arabidopsis. Plant Physiol. 179: 640–655.
Lv, Q., Zhong, Y., Wang, Y., Wang, Z., Zhang, L., Shi, J., Wu, Z., Liu, Y., Mao, C., and Yi, K., 2014. SPX4 negatively regulates phosphate signaling and homeostasis through its interaction with PHR2 in rice. Plant Cell. 26: 1586–1597.
Maeda, D., Ashida, K., Iguchi, K., Chechetka, S. A., Hijikata, A., Okusako, Y., Deguchi, Y., Izui, K., and Hata, S., 2006. Knockdown of an arbuscular mycorrhiza-inducible phosphate transporter gene of Lotus japonicus suppresses mutualistic symbiosis. Plant. Cell Physiol. 47: 807–817.
Maharajan, T., Ceasar, S. A., Ajeesh krishna, T. P., Ramakrishnan, M., Duraipandiyan, V., Naif Abdulla, A. D., and Ignacimuthu, S., 2018. Utilization of molecular markers for improving the phosphorus efficiency in crop plants. Plant Breed. 137: 10–26.
Masoni, A., Ercoli, L., Mariotti, M., and Arduini, I., 2007. Post-anthesis accumulation and remobilization of dry matter, nitrogen and phosphorus in durum wheat as affected by soil type. Eur. J. Agron. 26: 179–186.
Meina, G., Wenyuan, R., Changying, L., Fangliang, H., Ming, Z., Yingyao, L., Yanan, Y., Xiaomeng, D., Yunrong, W., and Zhongchang, W., 2015. Integrative comparison of the role of the PHR1 subfamily in phosphate signaling and homeostasis in rice. Plant Physiol. 168: 1762–1776.
Miao, J., Sun, J., Liu, D., Li, B., Zhang, A., Li, Z., and Tong, Y., 2009. Characterization of the promoter of phosphate transporter TaPHT1. 2 differentially expressed in wheat varieties. J. Genet. Genomics. 36: 455–466.
Misson, J., Thibaud, M. C., Bechtold, N., Raghothama, K., and Nussaume, L., 2004. Transcriptional regulation and functional properties of Arabidopsis Pht1; 4, a high affinity transporter contributing greatly to phosphate uptake in phosphate deprived plants. Plant Mol. Biol. 55: 727–741.
Mitsukawa, N., Okumura, S., Shirano, Y., Sato, S., Kato, T., Harashima, S., and Shibata, D., 1997. Overexpression of an Arabidopsis thaliana high-affinity phosphate transporter gene in tobacco cultured cells enhances cell growth under phosphate-limited conditions. Proc. Natl. Acad. Sci. 94: 7098–7102.
Miura, K., Rus, A., Sharkhuu, A., Yokoi, S., Karthikeyan, A. S., Raghothama, K. G., Baek, D., Koo, Y. D., Jin, J. B., and Bressan R. A., 2005. The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc. Natl. Acad. Sci. 102: 7760–7765.
Młodzińska, E., and Zboińska, M., 2016. Phosphate uptake and allocation–a closer look at Arabidopsis thaliana L. and Oryza sativa L. Front. Plant Sci. 7: 1198.
Muchhal, U. S., Pardo, J. M., and Raghothama, K., 1996. Phosphate transporters from the higher plant Arabidopsis thaliana. Proc. Natl. Acad. Sci. 93: 10519–10523.
Mudge, S. R., Rae, A. L., Diatloff, E., and Smith, F. W., 2002. Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis. Plant J. 31: 341–353.
Mukatira, U. T., Liu, C., Varadarajan, D. K., and Raghothama, K. G., 2001. Negative regulation of phosphate starvation-induced genes. Plant Physiol. 127: 1854–1862.
Nagarajan, V. K., Jain, A., Poling, M. D., Lewis, A. J., Raghothama, K. G., and Smith, A. P., 2011. Arabidopsis Pht1; 5 mobilizes phosphate between source and sink organs, and influences the interaction between phosphate homeostasis and ethylene signaling. Plant Physiol. 156: 1149–1163.
Nagarajan, V. K., and Smith, A. P., 2011. Ethylene's role in phosphate starvation signaling: more than just a root growth regulator. Plant Cell Physiol. 53: 277–286.
Nagy, R., Karandashov, V., Chague, V., Kalinkevich, K., Tamasloukht, M. B., Xu, G., Jakobsen, I., Levy, A. A., Amrhein, N., and Bucher, M., 2005. The characterization of novel mycorrhiza‐specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant J. 42: 236–250.
Nagy, R., Vasconcelos, M., Zhao, S., McElver, J., Bruce, W., Amrhein, N., Raghothama, K., and Bucher, M., 2006. Differential regulation of five Pht1 phosphate transporters from maize (Zea mays L.). Plant Biol. 8: 186–197.
Nussaume, L., Kanno, S., Javot, H., Marin, E., Nakanishi, T. M., and Thibaud, M. C., 2011. Phosphate import in plants: focus on the PHT1 transporters. Front. Plant Sci. 2: 83.
Oelkers, E. H., and Valsami-Jones, E., 2008. Phosphate mineral reactivity and global sustainability. Elements 4: 83–87.
Ova, E. A., Kutman, U. B., Ozturk, L., and Cakmak, I., 2015. High phosphorus supply reduced zinc concentration of wheat in native soil but not in autoclaved soil or nutrient solution. Plant Soil. 393: 147–162.
Paszkowski, U., Kroken, S., Roux, C., and Briggs, S. P., 2002. Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. 99: 13324–13329.
Pedersen, B. P., Kumar, H., Waight, A. B., Risenmay, A. J., Roe-Zurz, Z., Chau, B. H., Schlessinger, A., Bonomi, M., Harries, W., and Sali, A., 2013. Crystal structure of a eukaryotic phosphate transporter. Nature 496: 533–536.
Penido, M. G. M., and Alon, U. S., 2012. Phosphate homeostasis and its role in bone health. Pediatr. Nephrol. 27: 2039–2048.
Péret, B., De Rybel, B, Casimiro, I., Benková, E., Swarup, R., Laplaze, L., Beeckman, T., and Bennett, M. J., 2009. Arabidopsis lateral root development: an emerging story. Trends Plant Sci. 14: 399–408.
Péret, B., Clément, M., Nussaume, L., and Desnos, T., 2011. Root developmental adaptation to phosphate starvation: better safe than sorry. Trends Plant Sci. 16: 442–450.
Pierzynski, G. M., and McDowell, R. W., 2005. Chemistry, cycling, and potential movement of inorganic phosphorus in soils. In Phosphorus: Agriculture and the Environment; Sims, J. T., and Sharpley A. N., Eds. American Society of Agronomy, Crop Science Society of America, Soil Science Society of America, Inc.: Madison, WI, pp 53–86.
Plaxton, W. C., 2004. Plant response to stress: biochemical adaptations to phosphate deficiency. In Encyclopedia of Plant and Crop Science; Goodman, R. M., Ed. Marcel Dekker: New York, NY, pp 976–980.
Plaxton, W. C., and Tran, H. T., 2011. Metabolic adaptations of phosphate-starved plants. Plant Physiol. 156: 1006–1015.
Poirier, Y., Thoma, S., Somerville, C., and Schiefelbein, J., 1991. Mutant of Arabidopsis deficient in xylem loading of phosphate. Plant Physiol. 97: 1087–1093.
Poirier, Y., and Bucher, M., 2002. Phosphate transport and homeostasis in Arabidopsis. In The Arabidopsis Book; Somerville, C. R., and Meyerowitz, E. M., Eds. American Society of Plant Biologists: Rockville, MD, pp e0024.
Popova, Y., Thayumanavan, P., Lonati, E., Agrochão, M., and Thevelein, J. M., 2010. Transport and signaling through the phosphate-binding site of the yeast Pho84 phosphate transceptor. Proc. Natl. Acad. Sci. 107: 2890–2895.
Preuss, C. P., Huang, C. Y., Gilliham, M., and Tyerman, S. D., 2010. Channel-like characteristics of the low-affinity barley phosphate transporter PHT1; 6 when expressed in Xenopus oocytes. Plant Physiol. 152: 1431–1441.
Pudake, R. N., Mehta, C. M., Mohanta, T. K., Sharma, S., Varma, A., and Sharma, A. K., 2017. Expression of four phosphate transporter genes from finger millet (Eleusine coracana L.) in response to mycorrhizal colonization and Pi stress. 3 Biotech 7: 17.
Puga, M. I., Mateos, I., Charukesi, R., Wang, Z., Franco-Zorrilla, J. M., de Lorenzo, L., Irigoyen, M. L., Masiero, S., Bustos, R., and Rodríguez, J., 2014. SPX1 is a phosphate-dependent inhibitor of Phosphate Starvation Response 1 in Arabidopsis. Proc. Natl. Acad. Sci. 111: 14947–14952.
Qin, L., Guo, Y., Chen, L., Liang, R., Gu, M., Xu, G., Zhao, J., Walk, T., and Liao, H., 2012. Functional characterization of 14 Pht1 family genes in yeast and their expressions in response to nutrient starvation in soybean. PLoS One 7: e47726.
Rae, A. L., Cybinski, D. H., Jarmey, J. M., and Smith, F. W., 2003. Characterization of two phosphate transporters from barley; evidence for diverse function and kinetic properties among members of the Pht1 family. Plant Mol. Biol. 53: 27–36.
Raghothama K., 1999. Phosphate acquisition. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 665–693.
Ramaekers, L., Remans, R., Rao, I. M., Blair, M. W., and Vanderleyden, J. 2010. Strategies for improving phosphorus acquisition efficiency of crop plants. Field Crops Research 117: 169–176.
Rausch, C., Daram, P., Brunner, S., Jansa, J., Laloi, M., Leggewie, G., Amrhein, N., and Bucher, M., 2001. A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414: 462–466.
Rausch, C., and Bucher M., 2002. Molecular mechanisms of phosphate transport in plants. Planta 216: 23–37.
Rausch, C., Zimmermann, P., Amrhein, N., and Bucher M., 2004. Expression analysis suggests novel roles for the plastidic phosphate transporter Pht2; 1 in auto‐and heterotrophic tissues in potato and Arabidopsis. Plant J. 39: 13–28.
Remy, E., Cabrito, T., Batista, R., Teixeira, M., Sá‐Correia, I., and Duque, P., 2012. The Pht1; 9 and Pht1; 8 transporters mediate inorganic phosphate acquisition by the Arabidopsis thaliana root during phosphorus starvation. New Phytol. 195: 356–371.
Ren, F., Guo, Q. Q., Chang, L. L., Chen, L., Zhao, C. Z., Zhong, H., and Li, X. B., 2012. Brassica napus PHR1 gene encoding a MYB-like protein functions in response to phosphate starvation. PLoS One 7: 665.
Ribot, C., Zimmerli, C., Farmer, E. E., Reymond, P., and Poirier, Y., 2008. Induction of the Arabidopsis PHO1; H10 gene by 12-oxo-phytodienoic acid but not jasmonic acid via a coronatine insensitive 1-dependent pathway. Plant Physiol. 147: 696–706.
Richardson, A. E., Hocking, P. J., Simpson, R. J., and George, T. S., 2009. Plant mechanisms to optimise access to soil phosphorus. Crop Pasture Sci. 60: 124–143.
Rouached, H., Stefanovic, A., Secco, D., Bulak Arpat, A., Gout, E., Bligny, R., and Poirier, Y., 2011. Uncoupling phosphate deficiency from its major effects on growth and transcriptome via PHO1 expression in Arabidopsis. Plant J. 65: 557–570.
Rubio, V., Linhares, F., Solano, R., Martín, A. C., Iglesias, J., Leyva, A., and Paz-Ares, J., 2001. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev. 15: 2122–2133.
Samyn, D. R., Ruiz-Pávon, L., Andersson, M. R., Popova, Y., Thevelein, J. M., and Persson, B. L., 2012. Mutational analysis of putative phosphate-and proton-binding sites in the Saccharomyces cerevisiae Pho84 phosphate: H + transceptor and its effect on signalling to the PKA and PHO pathways. Biochem. J. 445: 413–422.
Sattari, S. Z., Bouwman, A. F., Giller, K. E., and Van Ittersum, M. K. 2012. Residual soil phosphorus as the missing piece in the global phosphorus crisis puzzle. Proc. Natl. Acad. Sci. 109: 6348–6353.
Sara Adrián L., de Andrade R. G. B., and Léia Menna Silveira B. A., 2017. Low mycorrhiza colonization changed phosphate transporter expression without altering P content in phosphorus-starved soybean plants. UNICAMP, Instituto de Biologia. 1–2. doi:10.13140/RG.2.2.32338.86724.
Sawers, R. J., Svane, S. F., Quan, C., Grønlund, M., Wozniak, B., Gebreselassie, M. N., González‐Muñoz, E., Montes, R. A. C., Baxter, I., and Goudet, J., 2017. Phosphorus acquisition efficiency in arbuscular mycorrhizal maize is correlated with the abundance of root‐external hyphae and the accumulation of transcripts encoding PHT1 phosphate transporters. New Phytol. 214: 632–643.
Scholz, R., and Wellmer, F. W., 2016. Comment on: “Recent revisions of phosphate rock reserves and resources: a critique” by Edixhoven et al. (2014)–clarifying comments and thoughts on key conceptions, conclusions and interpretation to allow for sustainable action. Earth Syst. Dynam. 7: 103–117.
Schünmann, P., Richardson, A., Smith, F., and Delhaize, E., 2004a. Characterization of promoter expression patterns derived from the Pht1 phosphate transporter genes of barley (Hordeum vulgare L.). J. Exp. Bot. 55: 855–865.
Schünmann, P. H., Richardson, A. E., Vickers, C. E., and Delhaize, E., 2004b. Promoter analysis of the barley Pht1; 1 phosphate transporter gene identifies regions controlling root expression and responsiveness to phosphate deprivation. Plant Physiol. 136: 4205–4214.
Secco, D., Baumann, A., and Poirier, Y., 2010. Characterization of the rice PHO1 gene family reveals a key role for OsPHO1; 2 in phosphate homeostasis and the evolution of a distinct clade in dicotyledons. Plant Physiol. 152: 1693–1704.
Secco, D., Wang, C., Shou, H., and Whelan, J., 2012. Phosphate homeostasis in the yeast Saccharomyces cerevisiae, the key role of the SPX domain-containing proteins. FEBS Lett. 586: 289–295.
Secco, D., Jabnoune, M., Walker, H., Shou, H., Wu, P., Poirier, Y., and Whelan, J., 2013. Spatio-temporal transcript profiling of rice roots and shoots in response to phosphate starvation and recovery. Plant Cell. 25: 4285–4304.
Seo, H. M., Jung, Y., Song, S., Kim, Y., Kwon, T., Kim, D. H., Jeung, S. J., Yi, Y. B., Yi, G., and Nam, M. H., 2008. Increased expression of OsPT1, a high-affinity phosphate transporter, enhances phosphate acquisition in rice. Biotechnol. Lett. 30: 1833–1838.
Sharma, N. C., and Sahi S. V., 2011. Enhanced organic phosphorus assimilation promoting biomass and shoot P hyperaccumulations in Lolium multiflorum grown under sterile conditions. Environ. Sci. Technol. 45: 10531–10537.
Shen, J., Yuan, L., Zhang, J., Li, H., Bai, Z., Chen, X., Zhang, W., and Zhang, F., 2011. Phosphorus dynamics: from soil to plant. Plant Physiol. 156: 997–1005.
Shi, S., Wang, D., Yan, Y., Zhang, F., Wang, H., Gu, M., Sun, S., and Xu, G., 2013. Function of phosphate transporter OsPHT2; 1 in improving phosphate utilization in rice. Chinese J. Rice Sci. 27: 457–465.
Shin, H., Shin, H. S., Dewbre, G. R., and Harrison, M. J., 2004. Phosphate transport in Arabidopsis: Pht1; 1 and Pht1; 4 play a major role in phosphate acquisition from both low‐and high‐phosphate environments. Plant J. 39: 629–642.
Shin, H., Shin, H. S., Chen, R., and Harrison, M. J., 2006. Loss of At4 function impacts phosphate distribution between the roots and the shoots during phosphate starvation. Plant J. 45: 712–726.
Shu, B., Xia, R. X., and Wang, P., 2012. Differential regulation of Pht1 phosphate transporters from trifoliate orange (Poncirus trifoliata L. Raf) seedlings. Sci. Hortic. 146: 115–123.
Shukla, V., Kaur, M., Aggarwal, S., Bhati, K. K., Kaur, J., Mantri, S., and Pandey, A. K., 2016. Tissue specific transcript profiling of wheat phosphate transporter genes and its association with phosphate allocation in grains. Sci. Rep. 6: 39293.
Silber, A., Ben-Jaacov, J., Ackerman, A., Bar-Tal, A., Levkovitch, I., Matsevitz-Yosef, T., Swartzberg, D., Riov, J, and Granot, D., 2002. Interrelationship between phosphorus toxicity and sugar metabolism in Verticordia plumosa L. Plant Soil. 245: 249–260.
Sisaphaithong, T., Kondo, D., Matsunaga, H., Kobae, Y., and Hata, S., 2012. Expression of plant genes for arbuscular mycorrhiza-inducible phosphate transporters and fungal vesicle formation in sorghum, barley, and wheat roots. Biosci. Biotechnol. Biochem. 76: 2364–2367.
Smith, F. W., Cybinski, D. H., and Rae, A. L., 1999. Regulation of expression of genes encoding phosphate transporters in barley roots. In: GisselNielsen, G., and Jensen, A., Eds. Plant Nutrition-Molecular Biology and Genetics. Proceedings of the Sixth International Symposium on Genetics and Molecular Biology of Plant Nutrition. Kluwer Academic Publishers: Dordrecht; Springer: The Netherlands, pp 145–150.
Smith, S. E., Dickson, S., and Smith, F. A., 2001. Nutrient transfer in arbuscular mycorrhizas: how are fungal and plant processes integrated? Funct. Plant Biol. 28: 685–696.
Smith, F. W., Mudge, S. R., Rae, A. L., and Glassop, D., 2003. Phosphate transport in plants. Plant Soil. 248: 71–83.
Smith, A. P., Jain, A., Deal, R. B., Nagarajan, V. K., Poling, M. D., Raghothama, K. G., and Meagher, R. B., 2010. Histone H2A. Z regulates the expression of several classes of phosphate starvation response genes but not as a transcriptional activator. Plant Physiol. 152: 217–225.
Smith, A. P., Nagarajan, V. K., and Raghothama, K. G., 2011. Arabidopsis Pht1; 5 plays an integral role in phosphate homeostasis. Plant Signal. Behav. 6: 1676–1678.
Smith, F. A., and Smith, S. E., 2011. What is the significance of the arbuscular mycorrhizal colonisation of many economically important crop plants? Plant Soil. 348: 63–79.
Stefanovic, A., Ribot, C., Rouached, H., Wang, Y., Chong, J., Belbahri, L., Delessert, S., and Poirier, Y., 2007. Members of the PHO1 gene family show limited functional redundancy in phosphate transfer to the shoot, and are regulated by phosphate deficiency via distinct pathways. Plant J. 50: 982–994.
Stefanovic, A., Arpat, A. B., Bligny, R., Gout, E., Vidoudez, C., Bensimon, M., and Poirier, Y., 2011. Over‐expression of PHO1 in Arabidopsis leaves reveals its role in mediating phosphate efflux. Plant J. 66: 689–699.
Su, T., Xu, Q., Zhang, F. C., Chen, Y., Li, L. Q., Wu, W. H., and Chen, Y. F., 2015. WRKY42 modulates phosphate homeostasis through regulating phosphate translocation and acquisition in Arabidopsis. Plant Physiol. 167: 1579–1591.
Sun, S., Gu, M., Cao, Y., Huang, X., Zhang, X., Ai, P., Zhao, J., Fan, X., and Xu, G., 2012. A constitutive expressed phosphate transporter, OsPht1; 1, modulates phosphate uptake and translocation in Pi-replete rice. Plant Physiol. 159: 1571–1581.
Sun, T., Li, M., Shao, Y., Yu, L., and Ma, F., 2017. Comprehensive genomic identification and expression analysis of the phosphate transporter (PHT) gene family in apple. Front. Plant Sci. 8: 426.
Takabatake, R., Hata, S., Taniguchi, M., Kouchi, H., Sugiyama, T., and Izui, K., 1999. Isolation and characterization of cDNAs encoding mitochondrial phosphate transporters in soybean, maize, rice, and Arabidopsis. Plant Mol. Biol. 40: 479–486.
Tamura, Y., Kobae, Y., Mizuno, T., and Hata, S., 2012. Identification and expression analysis of arbuscular mycorrhiza-inducible phosphate transporter genes of soybean. Biosci. Biotechnol. Biochem. 76: 309–313.
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731–2739.
Teng, W., Zhao, Y. Y., Zhao, X. Q., He, X., Ma, W. Y., Deng, Y., Chen, X. P., and Tong, Y. P., 2017. Genome-wide identification, characterization, and expression analysis of PHT1 phosphate transporters in wheat. Front. Plant Sci. 8: 543.
Tian, H., Drijber, R. A., Li, X., Miller, D. N., and Wienhold, B. J., 2013. Arbuscular mycorrhizal fungi differ in their ability to regulate the expression of phosphate transporters in maize (Zea mays L.). Mycorrhiza. 23: 507–514.
Tian, H., Yuan, X., Duan, J., Li, W., Zhai, B., and Gao, Y., 2017. Influence of nutrient signals and carbon allocation on the expression of phosphate and nitrogen transporter genes in winter wheat (Triticum aestivum L.) roots colonized by arbuscular mycorrhizal fungi. PLoS One 12: e0172154.
Torabi, S., Wissuwa, M., Heidari, M., Naghavi, M. R., Gilany, K., Hajirezaei, M. R., Omidi, M., Yazdi-Samadi, B., Ismail, A. M., and Salekdeh, G. H., 2009. A comparative proteome approach to decipher the mechanism of rice adaptation to phosphorous deficiency. Proteomics 9: 159–170.
Tran, H. T., Hurley, B. A., and Plaxton, W. C. 2010. Feeding hungry plants: the role of purple acid phosphatases in phosphate nutrition. Plant Sci. 179: 14–27.
Valat, L., Deglène-Benbrahim, L., Kendel, M., Hussenet, R., Le Jeune, C., Schellenbaum, P., and Maillot, P., 2018. Transcriptional induction of two phosphate transporter 1 genes and enhanced root branching in grape plants inoculated with Funneliformis mosseae. Mycorrhiza. 28: 179–185.
Van Kauwenbergh, S. J., Stewart, M., Mikkelsen, R. 2013. World reserves of phosphate rock… a dynamic and unfolding story. Better Crops. 97: 18–20.
Vance, C. P., Uhde-Stone, C., and Allan, D. L., 2003. Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol. 157: 423–447.
Versaw, W. K., and Harrison, M. J., 2002. A chloroplast phosphate transporter, PHT2; 1, influences allocation of phosphate within the plant and phosphate-starvation responses. Plant Cell. 14: 1751–1766.
Volpe, V., Giovannetti, M., Sun, X. G., Fiorilli, V., and Bonfante, P., 2016. The phosphate transporters LjPT4 and MtPT4 mediate early root responses to phosphate status in non mycorrhizal roots. Plant, Cell Environ. 39: 660–671.
Walder, F., Brulé, D., Koegel, S., Wiemken, A., Boller, T., and Courty, P. E., 2015. Plant phosphorus acquisition in a common mycorrhizal network: regulation of phosphate transporter genes of the Pht1 family in sorghum and flax. New Phytol. 205: 1632–1645.
Wang, X., Shen, J., and Liao, H., 2010. Acquisition or utilization, which is more critical for enhancing phosphorus efficiency in modern crops? Plant Sci. 179: 302–306.
Wang, C., Huang, W., Ying, Y., Li, S., Secco, D., Tyerman, S., Whelan, J., and Shou, H., 2012. Functional characterization of the rice SPX‐MFS family reveals a key role of OsSPX‐MFS1 in controlling phosphate homeostasis in leaves. New Phytol. 196: 139–148.
Wang, J., Sun, J., Miao, J., Guo, J., Shi, Z., He, M., Chen, Y., Zhao, X., Li, B., and Han, F., 2013a. A phosphate starvation response regulator Ta-PHR1 is involved in phosphate signalling and increases grain yield in wheat. Ann. Bot. 111: 1139–1153.
Wang, X., Bai, J., Liu, H., Sun, Y., Shi, X., and Ren, Z., 2013b. Overexpression of a maize transcription factor ZmPHR1 improves shoot inorganic phosphate content and growth of Arabidopsis under low-phosphate conditions. Plant Mol. Biol. Rep. 31: 665–677.
Wang, H., Xu, Q., Kong, Y. H., Chen, Y., Duan, J. Y., Wu, W. H., and Chen, Y. F., 2014a. Arabidopsis WRKY45 transcription factor activates PHT1; 1 expression in response to phosphate starvation. Plant Physiol. 164: 2020–2029.
Wang, X., Wang, Y., Piñeros, M. A., Wang, Z., Wang, W., Li, C., Wu, Z., Kochian, L. V., and Wu, P., 2014b. Phosphate transporters OsPHT1; 9 and OsPHT1; 10 are involved in phosphate uptake in rice. Plant Cell. Environ. 37: 1159–1170.
Wang, Z., Ruan, W., Shi, J., Zhang, L., Xiang, D., Yang, C., Li, C., Wu, Z., Liu, Y., and Yu, Y., 2014c. Rice SPX1 and SPX2 inhibit phosphate starvation responses through interacting with PHR2 in a phosphate-dependent manner. Proc. Natl. Acad. Sci. 111: 14953–14958.
Wang, F., Rose, T., Jeong, K., Kretzschmar, T., and Wissuwa, M., 2015. The knowns and unknowns of phosphorus loading into grains, and implications for phosphorus efficiency in cropping systems. J. Exp. Bot. 67: 1221–1229.
Wang, D., Lv, S., Jiang, P., and Li, Y., 2017. Roles, regulation, and agricultural application of plant phosphate transporters. Front. Plant Sci. 8: 817.
Willmann, M., Gerlach, N., Buer, B., Polatajko, A., Nagy, R., Koebke, E., Jansa, J., Flisch, R., and Bucher, M., 2013. Mycorrhizal phosphate uptake pathway in maize: vital for growth and cob development on nutrient poor agricultural and greenhouse soils. Front. Plant Sci. 4: 533.
Wu, Z., Zhao, J., Gao, R., Hu, G., Gai, J., Xu, G., and Xing, H., 2011. Molecular cloning, characterization and expression analysis of two members of the Pht1 family of phosphate transporters in Glycine max. PLoS One 6: e19752.
Xiao, K., Liu, J., Dewbre, G., Harrison, M., and Wang, Z. Y., 2006. Isolation and characterization of root‐specific phosphate transporter promoters from Medicago truncatula. Plant Biol. 8: 439–449.
Xu, G. h., Chague, V., Melamed-Bessudo, C., Kapulnik, Y., Jain, A., Raghothama, K. G., Levy, A. A., and Silber, A., 2007. Functional characterization of LePT4: a phosphate transporter in tomato with mycorrhiza-enhanced expression. J. Exp. Bot. 58: 2491–2501.
Yang, S. Y., Grønlund, M., Jakobsen, I., Grotemeyer, M. S., Rentsch, D., Miyao, A., Hirochika, H., Kumar, C. S., Sundaresan, V., and Salamin, N., 2012. Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the phosphate transporter 1 gene family. Plant Cell. 24: 4236–4251.
Yang, T., Hao, L., Yao, S., Zhao, Y., Lu, W., and Xiao, K., 2016. TabHLH1, a bHLH-type transcription factor gene in wheat, improves plant tolerance to Pi and N deprivation via regulation of nutrient transporter gene transcription and ROS homeostasis. Plant Physiol. Biochem. 104: 99–113.
Ye, Y., Yuan, J., Chang, X., Yang, M., Zhang, L., Lu, K., and Lian, X., 2015. The phosphate transporter gene OsPht1; 4 is involved in phosphate homeostasis in rice. PLoS One 10: e0126186.
Yi, K., Wu, Z., Zhou, J., Du, L., Guo, L., Wu, Y., and Wu, P., 2005. OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice. Plant Physiol. 138: 2087–2096.
Yuan, H., and Liu, D., 2008. Signaling components involved in plant responses to phosphate starvation. Journal of Integrative Plant Biol. 50: 849–859.
Yue, W., Ying, Y., Wang, C., Zhao, Y., Dong, C., Whelan, J., and Shou, H., 2017. Os NLA 1, a RING‐type ubiquitin ligase, maintains phosphate homeostasis in Oryza sativa via degradation of phosphate transporters. Plant J. 90: 1040–1051.
Zhang, C., Meng, S., Li, M., and Zhao, Z., 2016. Genomic identification and expression analysis of the phosphate transporter gene family in poplar. Front. Plant Sci. 7: 1398.
Zhang, F., Sun, Y., Pei, W., Jain, A., Sun, R., Cao, Y., Wu, X., Jiang, T., Zhang, L., and Fan, X., 2015. Involvement of O s P ht1; 4 in phosphate acquisition and mobilization facilitates embryo development in rice. Plant J. 82: 556–569.
Zhang, J., Guo, S., Ren, Y., Zhang, H., Gong, G., Zhou, M., Wang, G., Zong, M., He, H., and Liu, F., 2017. High‐level expression of a novel chromoplast phosphate transporter ClPHT4; 2 is required for flesh color development in watermelon. New Phytol. 213: 1208–1221.
Zhang, L., Hu, B., Li, W., Che, R., Deng, K., Li, H., Yu, F., Ling, H., Li, Y., and Chu, C., 2014. OsPT2, a phosphate transporter, is involved in the active uptake of selenite in rice. New Phytol. 201: 1183–1191.
Zheng, C., Zhang, J., and Li, X., 2013. Phosphorus supply level affects the regulation of phosphorus uptake by different arbuscular mycorrhizal fungal species in a highly P-efficient backcross maize line. Crop Pasture Sci. 64: 881–891.
Zhu, W., Miao, Q., Sun, D., Yang, G., Wu, C., Huang, J., and Zheng, C., 2012. The mitochondrial phosphate transporters modulate plant responses to salt stress via affecting ATP and gibberellin metabolism in Arabidopsis thaliana. PLoS One 7: e43530.